Deletion of mitochondrial anchoring protects dysmyelinating shiverer: Implications for progressive MS

Journal of Neuroscience

Volumn 35, Issue 13, 2015, Pages 5293-5306

  Joshi, Dinesh C ^a   Zhang, Chuan Li ^a   Lin, Tien Min ^a   Gusain, Anchal ^a   Harris, Melissa G ^a   Tree, Esther ^a   Yin, Yewin ^a   Wu, Connie ^a   Sheng, Zu Hang ^b   Dempsey, Robert J ^a   Fabry, Zsuzsanna ^a   Chiu, Shing Yan ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Axonal degeneration; Mitochondria; Multiple sclerosis; Oxidative stress; Syntaphilin

Indexed keywords

MITOCHONDRIAL PROTEIN; SYNTAPHILIN; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; SNPH PROTEIN, MOUSE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PROTECTION; CEREBELLUM; CONTROLLED STUDY; DEMYELINATION; DISEASE COURSE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE DELETION; GRAY MATTER; IMMUNOHISTOCHEMISTRY; LIFE EXTENSION; MITOCHONDRION; MORPHOMETRICS; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RESPIRATORY CHAIN; SHIVERER MOUSE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WHITE MATTER INJURY; ANIMAL; DEFICIENCY; DISEASE MODEL; GENETICS; INBRED MOUSE STRAIN; KNOCKOUT MOUSE; METABOLISM; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; PATHOLOGY; SURVIVAL; ULTRASTRUCTURE; WHITE MATTER;

ANIMALS; CEREBELLUM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GRAY MATTER; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; OXIDATIVE STRESS; SURVIVAL ANALYSIS; WHITE MATTER;

EID: 84929346699     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3859-14.2015     Document Type: Article

References (37)

1. Andrews H, White K, Thomson C, Edgar J, Bates D, Griffiths I, Turnbull D, Nichols P (2006) Increased axonal mitochondrial activity as an adaptation to myelin deficiency in the Shiverer mouse. J Neurosci Res 83:1533–1539.CrossRef Medline
2. Ashrafi G, Schlehe JS, LaVoie MJ, Schwarz TL (2014) Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J Cell Biol 206:655–670.CrossRef Medline
3. Basso AS, Frenkel D, Quintana FJ, Costa-Pinto FA, Petrovic-Stojkovic S, Puckett L, Monsonego A, Bar-Shir A, Engel Y, Gozin M, Weiner HL (2008) Reversal of axonal loss and disability in a mouse model of progressive multiple sclerosis. J Clin Invest 118:1532–1543.CrossRef Medline
4. Campbell GR, Ziabreva I, Reeve AK, Krishnan KJ, Reynolds R, Howell O, Lassmann H, Turnbull DM, Mahad DJ (2011) Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann Neurol 69:481– 492.CrossRef Medline
5. Davies AL, Desai RA, Bloomfield PS, McIntosh PR, Chapple KJ, Linington C, Fairless R, Diem R, Kasti M, Murphy MP, Smith KJ (2013) Neurological deficits caused by tissue hypoxia in neuroinflammatory disease. Ann Neurol 74:815–825.CrossRef Medline
6. Forte M, Gold BG, Marracci G, Chaudhary P, Basso E, Johnsen D, Yu X, Fowlkes J, Rahder M, Stem K, Bernardi P, Bourdette D (2007) Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Proc Natl Acad Sci U S A 104:7558–7563.CrossRef Medline
7. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610–1613.CrossRef Medline
8. Haider L, Fischer MT, Frischer JM, Bauer J, Höftberger R, Botond G, Esterbauer H, Binder CJ, Witztum JL, Lassmann H (2011) Oxidative damage in multiple sclerosis lesions. Brain 134:1914–1924.CrossRef Medline
9. Hulst HE, Geurts JJ (2011) Gray matter imaging in multiple sclerosis: what have we learned? BMC Neurol 11:153.CrossRef Medline
10. Inglese M, Oesingmann N, Casaccia P, Fleysher L (2011) Progressive multiple sclerosis and gray matter pathology: an MRI perspective. Mt Sinai J Med 78:258–267.CrossRef Medline
11. Inoue Y, Nakamura R, Mikoshiba K, Tsukada Y (1981) Fine structure of the central myelin sheath in the myelin deficient mutant Shiverer mouse, with special reference to the pattern of myelin formation by oligodendroglia. Brain Res 219:85–94.CrossRef Medline
12. Iwai M, Liu HW, Chen R, Ide A, Okamoto S, Hata R, Sakanaka M, Shiuchi T, Horiuchi M (2004) Possible inhibition of focal cerebral ischemia by angiotensin II type 2 receptor stimulation. Circulation 110:843–848.CrossRef Medline
13. Kageyama Y, Zhang Z, Roda R, Fukaya M, Wakabayashi J, Wakabayashi N, Kensler TW, Reddy PH, Iijima M, Sesaki H (2012) Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J Cell Biol 197:535–551.CrossRef Medline
14. Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH (2008) Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132:137–148.CrossRef Medline
15. Lao G, Scheuss V, Gerwin CM, Su Q, Mochida S, Rettig J, Sheng ZH (2000) Syntaphilin: a syntaxin-1 clamp that controls SNARE assembly. Neuron 25:191–201.CrossRef Medline
16. Lassmann H, van Horssen J, Mahad D (2012) Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol 8:647–656.CrossRef Medline
17. Loers G, Aboul-Enein F, Bartsch U, Lassmann H, Schachner M (2004) Comparison of myelin, axon, lipid, and immunopathology in the central nervous system of differentially myelin-compromised mutant mice: a morphological and biochemical study. Mol Cell Neurosci 27:175–189.CrossRef Medline
18. MacKenzie-Graham A, Tiwari-Woodruff SK, Sharma G, Aguilar C, Vo KT, Strickland LV, Morales L, Fubara B, Martin M, Jacobs RE, Johnson GA, Toga AW, Voskuhl RR (2009) Purkinje cell loss in experimental autoimmune encephalomyelitis. Neuroimage 48:637–651.CrossRef Medline
19. Mahad DJ, Ziabreva I, Campbell G, Lax N, White K, Hanson PS, Lassmann H, Turnbull DM (2009) Mitochondrial changes within axons in multiple sclerosis. Brain 132:1161–1174.CrossRef Medline
20. Mao P, Manczak M, Shirendeb UP, Reddy PH (2013) MitoQ, a mitochondria-targeted antioxidant, delays disease progression and alleviates pathogenesis in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis. Biochim Biophys Acta 1832:2322– 2331.CrossRef Medline
21. Molineaux SM, Engh H, de Ferra F, Hudson L, Lazzarini RA (1986) Recom bination within the myelin basic protein gene created the dysmyelinating shiverer mouse mutation. Proc Natl Acad Sci U S A 83:7542–7546.CrossRef Medline
22. Ohno N, Chiang H, Mahad DJ, Kidd GJ, Liu L, Ransohoff RM, Sheng ZH, Komuro H, Trapp BD (2014) Mitochondrial immobilization mediated by syntaphilin facilitates survival of demyelinated axons. Proc Natl Acad Sci U S A 111:9953–9958.CrossRef Medline
23. Pitt D, Gonzales E, Cross AH, Goldberg MP (2010) Dysmyelinated axons in shiverer mice are highly vulnerable to alpha-amino-3-hydroxy-5methylisoxazole-4-propionic acid (AMPA) receptor-mediated toxicity. Brain Res 1309:146–154.CrossRef Medline
24. Quick KL, Dugan LL (2001) Superoxide stress identifies neurons at risk in a model of ataxia-telangiectasia. Ann Neurol 49:627–635. MedlineCrossRef Medline
25. Roach A, Boylan K, Horvath S, Prusiner SB, Hood LE (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell 34:799–806.CrossRef Medline
26. Sheng ZH (2014) Mitochondrial trafficking and anchoring in neurons: New insight and implications. J Cell Biol 204:1087–1098.CrossRef Medline
27. Shichinohe H, Kuroda S, Yasuda H, Ishikawa T, Iwai M, Horiuchi M, Iwasaki Y (2004) Neuroprotective effects of the free radical scavenger Edaravone (MCI-186) in mice permanent focal brain ischemia. Brain Res 1029:200– 206.CrossRef Medline
28. Shields SD, Cheng X, Gasser A, Saab CY, Tyrrell L, Eastman EM, Iwata M, Zwinger PJ, Black JA, Dib-Hajj SD, Waxman SG (2012) A channelopathy contributes to cerebellar dysfunction in a model of multiple sclerosis. Ann Neurol 71:186–194.CrossRef Medline
29. Stys PK (2013) Pathoetiology of multiple sclerosis: are we barking up the wrong tree? F1000Prime Rep 5:20. MedlineCrossRef Medline
30. Stys PK, Zamponi GW, van Minnen J, Geurts JJ (2012) Will the real multiple sclerosis please stand up? Nat Rev Neurosci 13:507–514.CrossRef Medline
31. Su KG, Savino C, Marracci G, Chaudhary P, Yu X, Morris B, Galipeau D, Giorgio M, Forte M, Bourdette D (2012) Genetic inactivation of the p66 isoform of ShcA is neuroprotective in a murine model of multiple sclerosis. Eur J Neurosci 35:562–571.CrossRef Medline
32. Swingler RJ, Compston DA (1992) The morbidity of multiple sclerosis. Q J Med 83:325–337. MedlineCrossRef Medline
33. Tanji K, Bonilla E (2001) Optical imaging techniques (histochemical, immunohistochemical, and in situ hybridization staining methods) to visualize mitochondria. Methods Cell Biol 65:311–332.CrossRef Medline
34. Thompson AJ, Toosy AT, Ciccarelli O (2010) Pharmacological management of symptoms in multiple sclerosis: current approaches and future directions. Lancet Neurol 9:1182–1199. MedlineCrossRef Medline
35. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L (1998) Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338: 278–285.CrossRef Medline
36. Witte ME, Mahad DJ, Lassmann H, van Horssen J (2014) Mitochondrial dysfunction contributes to neurodegeneration in multiple sclerosis. Trends Mol Med 20:179–187.CrossRef Medline
37. Zambonin JL, Zhao C, Ohno N, Campbell GR, Engeham S, Ziabreva I, Schwarz N, Lee SE, Frischer JM, Turnbull DM, Trapp BD, Lassmann H, Franklin RJ, Mahad DJ (2011) Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis. Brain 134:1901– 1913.CrossRef Medline